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Does enteral nutrition through a percutaneous endoscopic gastrostomy, attenuate Helicobacter pylori colonization?: is it worth mentioning?

SUMMARY

OBJECTIVE:

In patients who experience difficulties in oral feeding, alimentary intake can be supported by creating direct access into the stomach through a percutaneous endoscopic gastrostomy. The present study purposed to compare naïve and exchanged percutaneous endoscopic gastrostomy tubes in terms of Helicobacter pylori infection and other clinical characteristics.

METHODS:

A total of 96 cases who underwent naïve or exchanged percutaneous endoscopic gastrostomy procedures with various indications were incorporated into the study. The patients’ demographic data, such as age and gender, etiology of percutaneous endoscopic gastrostomy, anti-HBs status, Helicobacter pylori status, the presence of atrophy and intestinal metaplasia, biochemical parameters, and lipid profiles, had been analyzed. In addition, the anti-HCV and anti-HIV statuses had also been evaluated.

RESULTS:

The most common indication for percutaneous endoscopic gastrostomy placement was dementia in 26 (27.08%) cases (p=0.033). The presence of Helicobacter pylori positivity was significantly lower in the exchange group compared to the naïve group (p=0.022). Total protein, albumin, and lymphocyte levels were significantly higher in the exchange group compared to the naïve group (both p=0.001), and the mean calcium, hemoglobin, and hematocrit levels were statistically significantly higher in the exchange group (p<0.001).

CONCLUSION:

Preliminary outcomes of the present study revealed that enteral nutrition attenuates the incidence of Helicobacter pylori infection. Considering the acute-phase reactant, the significantly lower ferritin values in the exchange group suggest that there is no active inflammatory process in the patients and that immunity is sufficient.

KEYWORDS:
Enteral nutrition; Gastrostomy; Immune system; Helicobacter pylori ; Pathology

INTRODUCTION

Patients who experience difficulties with oral feeding often require enteral or parenteral nutrition. In some cases, oral intake can even be dangerous in cases of obstructive or neurological conditions11 Kurien M, Penny H, Sanders DS. Impact of direct drug delivery via gastric access devices. Expert Opin Drug Deliv. 2015;12(3):455-63. https://doi.org/10.1517/17425247.2015.966683
https://doi.org/10.1517/17425247.2015.96...
. Enteral feeding has several advantages, including preserved enteral function, suppression of bacterial translocation, and reduced cost expenditure22 Jung SO, Moon HS, Kim TH, Park JH, Kim JS, Kang SH, et al. Nutritional impact of percutaneous endoscopic gastrostomy: a retrospective single-center study. Korean J Gastroenterol. 2022;79(1):12-21. https://doi.org/10.4166/kjg.2021.086
https://doi.org/10.4166/kjg.2021.086...
. In these cases, alimentary intake can be supported by creating direct access into the stomach through a percutaneous endoscopic gastrostomy (PEG) application. On a case-by-case basis, recently published European Society of Gastrointestinal Endoscopy guidelines recommends enteral feeding through a PEG tube application in cases for whom enteral feeding is required for longer than 3–4 weeks33 Masaki S, Kawamoto T. Comparison of long-term outcomes between enteral nutrition via gastrostomy and total parenteral nutrition in older persons with dysphagia: a propensity-matched cohort study. PLoS One. 2019;14(10):e0217120. https://doi.org/10.1371/journal.pone.0217120
https://doi.org/10.1371/journal.pone.021...
55 Arvanitakis M, Gkolfakis P, Despott EJ, Ballarin A, Beyna T, Boeykens K, et al. Endoscopic management of enteral tubes in adult patients - part 1: definitions and indications. European society of gastrointestinal endoscopy (ESGE) guideline. Endoscopy. 2021;53(1):81-92. PMID: 33260229. The 3–4-week cutoff is arbitrary and has been chosen to avoid numerous adverse events associated with percutaneous access, such as infections.

Percutaneous endoscopic gastrostomy was performed for the first time on 12 pediatric and 19 adult patients by Gauderer et al. using a mushroom catheter66 Gauderer MW, Ponsky JL, Izant RJ Jr. Gastrostomy without laparotomy: a percutaneous endoscopic technique. J Pediatr Surg. 1980;15(6):872-5. https://doi.org/10.1016/S0022-3468(80)80296-X
https://doi.org/10.1016/S0022-3468(80)80...
. Since then, multiple efforts have been made to improve the efficiency of the PEG procedure and reduce the rate of procedure-related complications. There has been a worldwide spread of this technique and an increase in indications for this medical approach. Of note, PEG allows the maintenance of normal physiological activities of the gastrointestinal tract and avoids long-term complications associated with intravenous nutritional support77 Fugazza A, Capogreco A, Cappello A, Nicoletti R, Rio DL, Galtieri PA, et al. Percutaneous endoscopic gastrostomy and jejunostomy: indications and techniques. World J Gastrointest Endosc. 2022;14(5):250-66. https://doi.org/10.4253/wjge.v14.i5.250
https://doi.org/10.4253/wjge.v14.i5.250...
. A gastric route through a PEG tube is advantageous over a jejunal approach due to its better tolerance, ease of the procedure, and possibility of being performed in a bedside model88 McClave SA, DiBaise JK, Mullin GE, Martindale RG. ACG clinical guideline: nutrition therapy in the adult hospitalized patient. Am J Gastroenterol. 2016;111(3):315-34. PMID: 26952578. Albumin and transferrin levels have been reported to improve after inserting a PEG tube in patients with dementia99 Nunes G, Santos CA, Santos C, Fonseca J. Percutaneous endoscopic gastrostomy for nutritional support in dementia patients. Aging Clin Exp Res. 2016;28(5):983-9. https://doi.org/10.1007/s40520-015-0485-2
https://doi.org/10.1007/s40520-015-0485-...
. Park et al.1010 Park RH, Allison MC, Lang J, Spence E, Morris AJ, Danesh BJ, et al. Randomised comparison of percutaneous endoscopic gastrostomy and nasogastric tube feeding in patients with persisting neurological dysphagia. BMJ. 1992;304(6839):1406-9. PMID: 1628013 reported that weight gained by patients who underwent the PEG procedure were significantly higher than those who underwent the nasogastric intubation. Moreover, PEG was associated with a significantly faster time to start feeding.

Although the benefits of PEG have been reported, several controversies and major concerns still exist regarding this procedure77 Fugazza A, Capogreco A, Cappello A, Nicoletti R, Rio DL, Galtieri PA, et al. Percutaneous endoscopic gastrostomy and jejunostomy: indications and techniques. World J Gastrointest Endosc. 2022;14(5):250-66. https://doi.org/10.4253/wjge.v14.i5.250
https://doi.org/10.4253/wjge.v14.i5.250...
. Previously placed PEG tubes can dislodge or be inadvertently removed, blocked, or damaged. PEG tube replacement is not performed infrequently1111 Sbeit W, Kadah A, Shahin A, Shbat S, Sbeit M, Khoury T. Scheduled percutaneous endoscopic gastrostomy tube replacement did not reduce PEG-related complications. Scand J Gastroenterol. 2021;56(11):1386-90. https://doi.org/10.1080/00365521.2021.1965209
https://doi.org/10.1080/00365521.2021.19...
. An endoscopic replacement is recommended as it becomes dislodged within a month after placement. However, bedside replacement is usually sufficient if the tube is dislodged after 4–6 weeks, when tract maturity is expected1212 Shah R, Shah M, Aleem A. Gastrostomy tube replacement. In: StatPearls. Treasure Island, FL: StatPearls Publishing; 2022. PMID: 29494029. To the best of our knowledge, the remarkable effect of enteral nutrition fluid in comparing patients who underwent PEG replacement and those who underwent PEG for the first time was that it caused a decrease in Helicobacter pylori colonization.

METHODS

A total of 96 patients who underwent naïve or exchanged PEG procedures in our clinic with various indications between January 01 and December 31, 2021 had been included in the study. Patients were divided into two groups as naïve and exchanged PEG, and the results were compared between the two groups. In addition, the demographic data, such as age and gender, etiology of PEG, anti-HBs, anti-HCV, anti-HIV, H. pylori status, the presence of atrophy and intestinal metaplasia, biochemical parameters, and lipid profiles, had been reevaluated in cases.

Percutaneous endoscopic gastrostomy tube placement

The technique of PEG tube placement had been performed in line with the British Society of Gastroenterology (BSG) practice guidelines1313 Westaby D, Young A, O’Toole P, Smith G, Sanders DS. The provision of a percutaneously placed enteral tube feeding service. Gut. 2010;59(12):1592-605. https://doi.org/10.1136/gut.2009.204982
https://doi.org/10.1136/gut.2009.204982...
. Briefly, PEG tube insertion using the pull technique had been performed under sterile conditions, and 2 g of ceftriaxone was administered intravenously as prophylaxis 30 min before the interventional procedure. The weight-adjusted midazolam and propofol were administered as sedation was required depending on the patient’s condition. After a skin shave was performed, a 1-cm skin incision just before insertion of the PEG was performed with a positive transillumination in all patients. The PEG tube insertion was performed by using the PEG 24® Pull Method (Cook Medical, Bloomington, IN, USA), and the tube was fixed using an exterior retention plate without sutures after its insertion. The dressing was made three times a day for the first 7 days after the procedure, and water was given through the PEG tube 24 h after the tube placement. Initially, 100 mL of food was injected to ensure that there were no complications. If this was tolerated, an additional 50 mL of food was added to the previous volume as described by Jung et al.33 Masaki S, Kawamoto T. Comparison of long-term outcomes between enteral nutrition via gastrostomy and total parenteral nutrition in older persons with dysphagia: a propensity-matched cohort study. PLoS One. 2019;14(10):e0217120. https://doi.org/10.1371/journal.pone.0217120
https://doi.org/10.1371/journal.pone.021...
.

Percutaneous endoscopic gastrostomy exchange procedure

If the PEG tube is not dislodged completely but has been clogged or malfunctioning, the old tube needs to be exchanged. If resistance is felt during the attempted removal of the old tube by gentle traction, it is best to remove the tube after the endoscopic cutting of the internal mushroom cap and removal of the rest of the tube through external puling. A similar-diameter PEG tube as the old tube should be used as an exchange tube. The final step in PEG tube exchange is to confirm the placement. For this purpose, water-soluble contrast is placed through the exchanged tube, and a contrast-enhanced abdominal X-ray is obtained to confirm placement in the stomach1414 Jacobson G, Brokish PA, Wrenn K. Percutaneous feeding tube replacement in the ED--are confirmatory x-rays necessary? Am J Emerg Med. 2009;27(5):519-24. https://doi.org/10.1016/j.ajem.2008.04.005
https://doi.org/10.1016/j.ajem.2008.04.0...
.

Statistical analysis

Data obtained in this study were statistically analyzed using the SPSS version 25.0 (SPSS, Statistical Package for Social Sciences, IBM Inc., Armonk, USA) statistical software. The normal distribution of the variables was tested using the Kolmogorov-–Smirnov method. Normally distributed continuous variables were compared between the groups with the independent t-test and non-normally distributed variables with the Mann-–Whitney U test. Categorical variables were compared using the χ22 Jung SO, Moon HS, Kim TH, Park JH, Kim JS, Kang SH, et al. Nutritional impact of percutaneous endoscopic gastrostomy: a retrospective single-center study. Korean J Gastroenterol. 2022;79(1):12-21. https://doi.org/10.4166/kjg.2021.086
https://doi.org/10.4166/kjg.2021.086...
test. Normally distributed continuous variables are expressed as mean±standard deviation and non-normally distributed variables are expressed as median (min–max) values. Categorical variables are given as a frequency (number, percentage), and p-values < 0.05 were considered statistically significant for the study.

RESULTS

A total of 96 patients who underwent placement or replacement (exchange) PEG procedures due to various etiologies in our clinic were included in the study. The patients were divided into two groups, namely, naïve and exchange. Patients with a PEG inserted before ≤1.5 months were considered to have naïve PEGs, while the others were included in the exchange group. Accordingly, the naïve group consisted of 44 cases, and the exchange group consisted of 52 cases. The median PEG exchange duration was 9 months (min–max: 0.5–6). Of all patients, 37 (38.5%) were male and 59 (61.5%) were female.

The median age was found to be 83 years (min–max: 35–96) in the exchange and 79 years (min–max: 26–95) in the naïve. Of the patients in the exchange, 14 (26.9%) were male and 38 (73.1%) were female, while in the naïve, 23 (52.3%) were male and 21 (47.7%) were female. There was a statistically significant difference between the two groups in terms of gender (p=0.020), while no significant difference was observed in terms of age (p=0.179). The most common indication for PEG placement was dementia in 26 (27.08%) cases (p=0.033). The other etiologies are shown in Figure 1.

Figure 1
Etiologies of the percutaneous endoscopic gastrostomy application.

When the clinical features of the patients were examined, the presence of H. pylori positivity was significantly lower in the exchange compared to the naïve (p=0.022). Clinical features of the patients are given in Table 1. Among laboratory parameters, glucose was significantly lower in the exchange group (p=0.05). Similarly, ferritin levels were statistically significantly lower in the exchange compared to the naïve (p=0.001). The exchange group’s lymphocyte count was significantly higher (p=0.001) (Table 2). Total protein and albumin levels were statistically significantly higher in the exchange compared to the naïve (both, p=0.001). The mean calcium, hemoglobin, and hematocrit levels were statistically significantly higher in the exchange (for all, p<0.001). The PNI value calculated as [albumin (g/dL)×10+lymphocyte (×109/mL)×0.005] was also statistically significantly higher in the exchange compared to the naïve (p<0.001).

Table 1
Clinicopathological features of the cases.
Table 2
Laboratory parameters of the cases.

DISCUSSION

Nutritional support is essential in patients who have a limited capacity to maintain their normal body weight through a normal diet77 Fugazza A, Capogreco A, Cappello A, Nicoletti R, Rio DL, Galtieri PA, et al. Percutaneous endoscopic gastrostomy and jejunostomy: indications and techniques. World J Gastrointest Endosc. 2022;14(5):250-66. https://doi.org/10.4253/wjge.v14.i5.250
https://doi.org/10.4253/wjge.v14.i5.250...
. Enteral nutrition is indicated for patients who have a functional gastrointestinal tract and whose oral nutritional intake is insufficient to meet the estimated nutritional needs1515 Hill A, Elke G, Weimann A. Nutrition in the intensive care unit-a narrative review. Nutrients. 2021;13(8):2851. https://doi.org/10.3390/nu13082851
https://doi.org/10.3390/nu13082851...
. The placement of a PEG tube is one of the most commonly used methods to provide enteral feeding. PEG is usually indicated when a period of inadequate nutritional intake exceeding 2–4 weeks is expected, such as in patients with malignancies (mainly head and neck) or neurological diseases (e.g., cerebrovascular stroke and brain hemorrhage)22 Jung SO, Moon HS, Kim TH, Park JH, Kim JS, Kang SH, et al. Nutritional impact of percutaneous endoscopic gastrostomy: a retrospective single-center study. Korean J Gastroenterol. 2022;79(1):12-21. https://doi.org/10.4166/kjg.2021.086
https://doi.org/10.4166/kjg.2021.086...
. Since its introduction, PEG has become a very well-established endoscopic procedure for the enteral feeding of patients.

In the present study, we evaluated the efficacy of the enteral feeding system by comparing naïve and exchanged PEGs. Our results indicated that enteral feeding was maintained through the PEG system. No evidence-based guidelines regarding the replacement of PEG tubes have been reported. Our study’s median PEG exchange duration was 9 months (0.5–6). Similarly, in a study by Bouchiba et al.1616 Bouchiba H, Jacobs MAJM, Bouma G, Ramsoekh D. Outcomes of push and pull percutaneous endoscopic gastrostomy placements in 854 patients: a single-center study. JGH Open. 2021;6(1):57-62. https://doi.org/10.1002/jgh3.12694
https://doi.org/10.1002/jgh3.12694...
the median follow-up was found to be 8.9 months. In our study, the median age was found to be 83 years (35–96) in the PEG exchange group, while Jung et al.22 Jung SO, Moon HS, Kim TH, Park JH, Kim JS, Kang SH, et al. Nutritional impact of percutaneous endoscopic gastrostomy: a retrospective single-center study. Korean J Gastroenterol. 2022;79(1):12-21. https://doi.org/10.4166/kjg.2021.086
https://doi.org/10.4166/kjg.2021.086...
reported the mean age of 77 years.

Helicobacter pylori is a gram-negative, microaerophilic, spiral-shaped, and active bacteria that possess the ability to colonize in gastric mucosa, causing histopathological alterations in some cases, such as persistent inflammation, even peptic ulcus, chronic active gastritis, mucosa-associated lymphoid tissue lymphoma, and gastric adenocarcinoma. H. pylori remains one of the most common bacterial infections in humans. It has been suggested that H. pylori infection may influence intake and caloric homeostasis1717 Ijaopo EO, Ijaopo RO. Tube feeding in individuals with advanced dementia: a review of its burdens and perceived benefits. J Aging Res. 2019;2019:7272067. https://doi.org/10.1155/2019/7272067
https://doi.org/10.1155/2019/7272067...
2222 Akyol T, Dülger A, Dirik Y, Şeker D, Serim VA, Hakyemez HA, et al. Prevalence of Helicobacter pylori infection in patients with Dementia who underwent percutaneous endoscopic gastrostomy (PEG) and the effect of preventive single dose ceftriaxone plus pantoprazole therapy on Helicobacter pylori infection. Med Sci Discov. 2022;9(3):149-52. https://doi.org/10.36472/msd.v9i3.686
https://doi.org/10.36472/msd.v9i3.686...
. It has been reported that the bacterial content of the gut and the presence of relevant antigens influence the rate of recovery of host pathophysiology induced by chronic H. pylori infection2323 Verdu EF, Bercik P, Huang XX, Lu J, Al-Mutawaly N, Sakai H, et al. The role of luminal factors in the recovery of gastric function and behavioral changes after chronic Helicobacter pylori infection. Am J Physiol Gastrointest Liver Physiol. 2008;295(4):G664-70. https://doi.org/10.1152/ajpgi.90316.2008
https://doi.org/10.1152/ajpgi.90316.2008...
. Histopathologically, a high ratio of gastric mucosa abnormalities, chronic active gastritis, and reactive gastropathy have been reported in cases with H. pylori colonization2121 Ozturk T, Sengul D, Sengul I. Helicobacter pylori and association between its positivity and anatomotopographic settlement in the stomach with the host age range. Ann Afr Med. 2021;20(1):1-8. https://doi.org/10.4103/aam.aam_69_19
https://doi.org/10.4103/aam.aam_69_19...
,2424 Lee I, Lee H, Kim M, Fukumoto M, Sawada S, Jakate S, et al. Ethnic difference of Helicobacter pylori gastritis: Korean and Japanese gastritis is characterized by male- and antrum-predominant acute foveolitis in comparison with American gastritis. World J Gastroenterol. 2005;11(1):94-8. https://doi.org/10.3748/wjg.v11.i1.94
https://doi.org/10.3748/wjg.v11.i1.94...
.

In the present study, H. pylori positivity was significantly lower in the exchange compared to the naïve (p=0.022). In addition, H. pylori prevalence varies concerning ethnicity and geographic regions worldwide1919 Sengul D, Sengul I. Frequency of Helicobacter pylori and relationship between location, six age groups and evaluation of pilot zone based borderline of 50-year age with histopathological Helicobacter pylori colonization grade. Bakirkoy Med J. 2018;14(4):381-8. https://doi.org/10.4274/BTDMJB.20180327085510
https://doi.org/10.4274/BTDMJB.201803270...
,2121 Ozturk T, Sengul D, Sengul I. Helicobacter pylori and association between its positivity and anatomotopographic settlement in the stomach with the host age range. Ann Afr Med. 2021;20(1):1-8. https://doi.org/10.4103/aam.aam_69_19
https://doi.org/10.4103/aam.aam_69_19...
. Lee et al.2424 Lee I, Lee H, Kim M, Fukumoto M, Sawada S, Jakate S, et al. Ethnic difference of Helicobacter pylori gastritis: Korean and Japanese gastritis is characterized by male- and antrum-predominant acute foveolitis in comparison with American gastritis. World J Gastroenterol. 2005;11(1):94-8. https://doi.org/10.3748/wjg.v11.i1.94
https://doi.org/10.3748/wjg.v11.i1.94...
reported that H. pylori positivity was detected in 48.3, 67.4, and 77.9% of Americans, Korean, and Japanese, respectively. They also stated the antrum location dominancy. In the study conducted in December 2018, Sengul and Sengul1919 Sengul D, Sengul I. Frequency of Helicobacter pylori and relationship between location, six age groups and evaluation of pilot zone based borderline of 50-year age with histopathological Helicobacter pylori colonization grade. Bakirkoy Med J. 2018;14(4):381-8. https://doi.org/10.4274/BTDMJB.20180327085510
https://doi.org/10.4274/BTDMJB.201803270...
,2121 Ozturk T, Sengul D, Sengul I. Helicobacter pylori and association between its positivity and anatomotopographic settlement in the stomach with the host age range. Ann Afr Med. 2021;20(1):1-8. https://doi.org/10.4103/aam.aam_69_19
https://doi.org/10.4103/aam.aam_69_19...
reported 55.2% overall positivity of H. pylori with the antrum dominancy, 57.9%, in our studied city region. Their reported positivity was between the positivity of American and Korean-Japan groups with the frequent location of the antrum, concerning the corpus.

Several markers are used to evaluate nutritional status in the enteral feeding system through a PEG. In the present study, glucose and ferritin levels were significantly lower in the exchange group (p<0.05). The lymphocyte count was significantly higher in the exchange group (p=0.001). Similarly, in a study by Jung et al.22 Jung SO, Moon HS, Kim TH, Park JH, Kim JS, Kang SH, et al. Nutritional impact of percutaneous endoscopic gastrostomy: a retrospective single-center study. Korean J Gastroenterol. 2022;79(1):12-21. https://doi.org/10.4166/kjg.2021.086
https://doi.org/10.4166/kjg.2021.086...
lymphocyte count was higher in the post-PEG group compared to the pre-PEG group.

In the present study, total protein and albumin levels were statistically significantly higher in the exchange group versus the naïve group (p=0.001). Total protein was also significantly higher in the post-PEG group in the Jung et al.22 Jung SO, Moon HS, Kim TH, Park JH, Kim JS, Kang SH, et al. Nutritional impact of percutaneous endoscopic gastrostomy: a retrospective single-center study. Korean J Gastroenterol. 2022;79(1):12-21. https://doi.org/10.4166/kjg.2021.086
https://doi.org/10.4166/kjg.2021.086...
study. The mean calcium, hemoglobin, and hematocrit levels were statistically significantly higher in the exchange group (for all, p<0.001). The PNI value was also significantly higher in the exchange group than in the naïve group (p<0.001). However, since this is the first study in the literature comparing naïve and exchange PEGs, we could not compare our findings exactly.

Study limitations

The main limitations of the current study include its retrospective nature and the relatively small number of patients. In addition, we could not measure pre-PEG values. However, given the lack of a similar study in the literature, we believe that our findings will serve as a guide for future, more comprehensive studies.

CONCLUSION

Our findings indicate that dementia was the most common etiology for PEG placement, enteral feeding was maintained, and this decreased the incidence of H. pylori infection. Total protein, glucose, albumin, and lymphocyte counts were statistically higher, while ferritin levels were significantly lower in the PEG exchange group, showing that enteral feeding was maintained and continued to provide nutritional support through PEG. To the best of our knowledge, this is the first study in the English literature stating that enteral nutrition through PEG might lead to attenuating H. pylori colonization. However, further comprehensive prospective studies are needed to confirm our findings.

  • Funding: none.

ACKNOWLEDGMENTS

The authors thank all the participants involved in this study.

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    » https://doi.org/10.1002/jgh3.12694
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Publication Dates

  • Publication in this collection
    21 Apr 2023
  • Date of issue
    2023

History

  • Received
    28 Dec 2022
  • Accepted
    04 Jan 2023
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